MIS-C and Cardiac

Conduction Abnormalities
Nak Hyun Choi, MD, Michael Fremed, MD, Thomas Starc, MD, Rachel Weller, MD, Eva Cheung, MD, Anne Ferris, MBBS,
Eric S. Silver, MD, Leonardo Liberman, MD

Multisystem inflammatory syndrome in children (MIS-C) has spread through the

OBJECTIVES: abstract
pediatric population during the coronavirus disease 2019 pandemic. Our objective for the
study was to report the prevalence of conduction anomalies in MIS-C and identify predictive
factors for the conduction abnormalities.
METHODS: We performed a single-center retrospective cohort study of pediatric patients
,21 years of age presenting with MIS-C over a 1-month period. We collected clinical
outcomes, laboratory findings, and diagnostic studies, including serial electrocardiograms, in
all patients with MIS-C to identify those with first-degree atrioventricular block (AVB) during
the acute phase and assess for predictive factors.
RESULTS: Thirty-two patients met inclusion criteria. Median age at admission was 9 years. Six of
32 patients (19%) were found to have first-degree AVB, with a median longest PR interval of
225 milliseconds (interquartile range 200–302), compared with 140 milliseconds
(interquartile range 80–178) in patients without first-degree AVB. The onset of AVB occurred
at a median of 8 days after the initial symptoms and returned to normal 3 days thereafter. No
patients developed advanced AVB, although 1 patient developed a PR interval .300
milliseconds. Another patient developed new-onset right bundle branch block, which resolved
during hospitalization. Cardiac enzymes, inflammatory markers, and cardiac function were not
associated with AVB development.
CONCLUSIONS: In our population, there is a 19% prevalence of first-degree AVB in patients with
MIS-C. All patients with a prolonged PR interval recovered without progression to high-degree
AVB. Patients admitted with MIS-C require close electrocardiogram monitoring during the
acute phase.

Division of Pediatric Cardiology, NewYork-Presbyterian Morgan Stanley Children’s Hospital, Columbia University WHAT’S KNOWN ON THIS SUBJECT: A novel disease
Irving Medical Center, New York, New York known as multisystem inflammatory syndrome in
children (MIS-C) has been increasingly prevalent in
Drs Choi and Liberman conceptualized and designed the study, drafted the initial manuscript, and pediatric patients with coronavirus disease 2019. Few
reviewed and revised the manuscript; Drs Fremed, Starc, Weller, Cheung, Ferris, and Silver critically data are available on the incidence of arrhythmia and
reviewed and revised the manuscript for important intellectual content; and all authors approved
cardiac involvement in children with MIS-C.
the final manuscript as submitted.
DOI: https://doi.org/10.1542/peds.2020-009738 WHAT THIS STUDY ADDS: Pediatric patients with MIS-C
may develop conduction anomalies, particularly first-
Accepted for publication Sep 4, 2020 degree atrioventricular block. Patients have elevated
Address correspondence to Leonardo Liberman, MD, Division of Pediatric Cardiology, NewYork- levels of cardiac and inflammatory markers, which are
Presbyterian Morgan Stanley Children’s Hospital, Columbia University Irving Medical Center, 3959 not associated with development of conduction
Broadway, CHN 2-255, New York, NY 10032. E-mail: ll202@cumc.columbia.edu abnormalities. First-degree atrioventricular block
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). typically returns to normal after the acute illness phase.
Copyright © 2020 by the American Academy of Pediatrics
To cite: Choi NH, Fremed M, Starc T, et al. MIS-C and
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to Cardiac Conduction Abnormalities. Pediatrics. 2020;146(6):
this article to disclose. e2020009738

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PEDIATRICS Volume 146, number 6, December 2020:e2020009738 ARTICLE
Since the first report of coronavirus Center Institutional Review Board. admission, which was reviewed daily
disease 2019 (COVID-19) on We conducted a retrospective cohort by a pediatric cardiologist. All
December 31, 2019, new disease study of all patients ,21 years of age statistical analyses were conducted in
manifestations and complications are presenting to NewYork-Presbyterian Stata software version 16 (Stata Corp,
continuing to appear in pediatric Morgan Stanley Children’s Hospital in College Station, TX). Clinical and
patients. Early studies in China New York City, New York, with demographic variables were
revealed that children of all ages were a clinical diagnosis of MIS-C between described by using summary
susceptible to severe acute April 15, 2020, and May 15, 2020. A statistics. All continuous data were
respiratory syndrome coronavirus 2 diagnosis of MIS-C was made by using presented as medians with ranges or
(SARS-CoV-2), the viral etiology of the case definition per the US Centers interquartile ranges (IQRs).
COVID-19.1 Compared with adults, for Disease Control and Prevention Categorical variables were presented
pediatric patients were more guidelines.3,4 The diagnosis of MIS-C as number (%). The Wilcoxon rank
commonly asymptomatic or had was made in patients ,21 years old test was used for univariable
benign respiratory and presenting with fever ($38.0°C for analyses. Variables with a P value
gastrointestinal symptoms.1 Recently, $24 hours or report of subjective ,.05 were considered statistically
a new study revealed an emergence fever lasting $24 hours), laboratory significant.
of Kawasaki disease–like evidence of inflammation ($1 of the
presentations in pediatric patients following: elevated C-reactive protein
with an active or recent diagnosis of level, erythrocyte sedimentation rate, RESULTS
COVID-19.2 The new syndrome, now fibrinogen level, procalcitonin level, Patient Characteristics
known as multisystem inflammatory d-dimer level, ferritin level, lactic acid
syndrome in children (MIS-C), has dehydrogenase level, or interleukin 6 Thirty-two patients were diagnosed
been most prevalent in regions highly level or elevated neutrophil count), with MIS-C. Demographic details of
burdened with COVID-19.2–4 and clinical severity requiring the study population are listed in
hospitalization. Patients had Table 1. The median age was 9 years
As a large academic institution in (range 1–20), and there were 17
multisystem ($2) organ involvement,
New York City at the epicenter of the (53%) male patients. A majority of
including the cardiac, renal,
COVID-19 pandemic, our institution patients (n = 22; 69%) were found to
respiratory, hematologic,
has cared for multiple patients with have negative results on the SARS-
gastrointestinal, dermatologic, or
MIS-C. During the clinical assessment CoV-2 PCR testing but positive results
neurologic system. Patients did not
and treatment of patients with MIS-C, on the COVID-19 serology testing. The
have a plausible alternative diagnosis
a subset of pediatric patients with PR remaining patients (n = 10; 31%) had
and had to have tested positive for
prolongation on the positive results on PCR testing. The
current or recent SARS-CoV-2
electrocardiogram (ECG), consistent majority of patients received both
infection by reverse transcription
with first-degree atrioventricular glucocorticoid (n = 30; 94%) and
polymerase chain reaction (PCR),
block (AVB), emerged. Although intravenous immunoglobulin (IVIg)
serology, or an antigen test.3,4 At our
a recent case report described an therapy (n = 29; 91%) during
institution, the serology testing does
adult with a high-degree AVB and hospitalization, whereas 13% (n = 4)
not differentiate between
a confirmed diagnosis of COVID-19 in of patients received anakinra,
immunoglobulin M and
the absence of MIS-C symptoms, to a recombinant human interleukin-1
immunoglobulin G; thus, a positive
our knowledge there has not been receptor antagonist.
serology test result does not clearly
a similar report in pediatric patients.5
define a resolved infection. ECGs were
Our primary aim for this study was to routinely obtained after admission ECG Findings
report the frequency of conduction according to our institution’s Of the 32 total patients, 6 had first-
anomalies in MIS-C and to characterize guidelines for workup of all patients degree AVB (19%) during
the presentation and clinical course for with MIS-C.6 First-degree AVB on the hospitalization, including 2 patients
the subset of patients who develop these ECG was defined as a PR interval on with PR prolongation on the initial
abnormalities. We also sought to identify a surface ECG .200 milliseconds ECG at presentation. None of the 6
predictive factors for conduction without associated disruption of patients progressed to advanced AVB
abnormalities in patients with MIS-C. atrial-to-ventricular conduction.7 All while on telemetry monitoring. The
ECGs were read by a pediatric median of the longest PR interval for
cardiologist using electronic calipers. patients who did not develop first-
METHODS All patients suspected of having MIS- degree AVB versus the patients who
The study was approved by the C were placed on continuous developed first-degree block, was 140
Columbia University Irving Medical telemetry monitoring during milliseconds (range: 80–178) vs 225

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2 CHOI et al
TABLE 1 Patient Characteristics findings in patients with first-degree
Patient Characteristics AVB included a prolonged QTc
Total No. patients 32
interval (n = 2), ectopic atrial rhythm
Age, y, median (range) 9 (1–20) (n = 2), ST elevation in inferior leads
Male sex, n (%) 17 (53) (n = 2), and nonspecific ST and T
COVID-19 laboratory testing, n (%) wave abnormalities (n = 5). Notably, 1
PCR negative result and serology positive result 22 (69) patient developed a new-onset right
PCR positive result and serology positive result 7 (22)
PCR positive result and serology result unknown 3 (9)
bundle branch block (RBBB) along
Treatment, n (%) with first-degree AVB on day 3 of
IVIg 29 (91) hospitalization, both of which
Glucocorticoids 30 (94) subsequently resolved by day 5
Anakinra 4 (13) (Fig 2). There was 1 patient who was
Initial ECG intervals, median (IQR)
HR, beats per minute 128 (102–143)
found to have profound PR
PR, ms 135 (121–160) prolongation of 302 milliseconds
QRS, ms 77 (72–86) (Fig 3). Two of the 6 patients with PR
QTc, ms 421 (398–434) prolongation had an initial QTc
HR, heart rate. interval of 476 milliseconds and
a QTc interval of 473 milliseconds in
the absence of medications
milliseconds (range: 200–302), who developed first-degree AVB. All prolonging the QTc interval. At the
respectively (P # .01). No patients patients underwent an ECG every 24 conclusion of the study, both patients’
developed tachyarrhythmias during to 48 hours until discharge. The onset QTc values became normal.
hospitalization. None of the patients of first-degree AVB occurred at
Additionally, abnormal ECG findings
with first-degree AVB received a median of 8 days after the initial
in patients without first-degree AVB
medications that prolonged the PR onset of symptoms (range: 5–10). The
included a prolonged QTc interval
interval, including b-blockers, time to resolution of PR prolongation
(n = 4), ectopic atrial rhythm (n = 1),
calcium channel blockers, or other occurred at a median of 3 days after
ST elevation or depression (n = 3), T
antiarrhythmic medications. the initial first-degree AVB (range:
wave inversions (n = 5), nonspecific
1–5). One patient’s prolonged PR
ST and/or T wave abnormalities (n =
Figure 1 reveals chronological PR interval did not resolve by the
14), nonspecific intraventricular
changes for the 6 patients with MIS-C conclusion of the study. Other ECG
conduction delay or right ventricular
conduction delay (n = 5), right axis
deviation (n = 5), and intermittent
premature ventricular complexes (n =
1). Four patients without first-degree
heart block had QTc intervals of 474,
486, 488, and 494 milliseconds,
which all normalized by the
conclusion of the study.

Hospitalization Findings
There was no statistical difference in
the rate of ICU admission during
hospitalization between those with
first-degree AVB and those without (4
of 6 [67%] and 21 of 26 [81%],
respectively; P = .46).
All patients diagnosed with MIS-C
underwent echocardiography during
hospitalization, and the left
ventricular ejection fraction (LVEF)
was measured. Univariable analyses
FIGURE 1 were completed by using the lowest
PR interval changes on serial ECGs during MIS-C from onset of illness. ejection fraction during the patient’s

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PEDIATRICS Volume 146, number 6, December 2020 3
 development of first-degree AVB. At
the time of the initial first-degree AVB
development, all patients had normal
electrolyte levels.

DISCUSSION
Since the initial report of COVID-19 in
December 2019, children with severe
complications requiring
hospitalization were relatively rare
during the first several months of the
pandemic. A recent surge in pediatric
patients with significant systemic
inflammatory response and
multiorgan dysfunction, with
symptoms overlapping with
Kawasaki disease, has shifted the
diagnostic and treatment paradigm
for the pediatric population.8,9 At our
institution, .30 patients were
admitted with a diagnosis of MIS-C
during the study period. From
a cardiovascular perspective, some
patients were noted to have
FIGURE 2 decreased cardiac function and
ECG findings in a 9-year-old boy. A, Initial 12-lead ECG on presentation revealing normal sinus rhythm conduction abnormalities.
with narrow QRS complexes. B, Twelve-lead ECG on day 3 of hospitalization revealing first-degree AVB
(PR of 200 milliseconds) with RBBB. Early reports in adult patients
revealed direct cardiac complications
of COVID-19, including arrhythmias,
hospitalization (Table 2). There were significantly different (53.5% [IQR:
acute myocardial injury, and
2 patients with a significantly 45–57] and 56.5% [IQR: 48–59],
myocarditis with circulatory
decreased LVEF (30% and 35%) in respectively; P = .32).
failure.10,11 In a recent study, an adult
the group without conduction
Cardiac and inflammatory markers patient was found to have high-
anomalies and none in the group with
were also obtained for all patients degree AVB in the setting of COVID-
PR prolongation. Despite these
during hospitalization, illustrated in 19 illness in the absence of MIS-C
outliers, the median LVEF for patients
symptoms.5 In our study, we analyzed
who had first-degree AVB, compared Table 2. No laboratory variable was
pediatric patients with a COVID-
with patients without, was not significantly associated with the
19–related inflammatory disease; our
patients with MIS-C exhibited
conduction abnormalities, including
first-degree AVB and RBBB.
AVB has been associated with
multiple infectious and inflammatory
diseases, such as Lyme disease, acute
rheumatic fever, and myocarditis.12–14
Occurring in 15% to 20% of patients,
a prolonged PR interval is a minor
criteria for diagnosis of acute
rheumatic fever.13,15 Our study
revealed a similar 19% incidence of
FIGURE 3 a prolonged PR interval in pediatric
Twelve-lead ECG revealing significant first-degree AVB with a PR interval of 302 milliseconds and patients with MIS-C. Previous studies
nonspecific T wave abnormalities in a 12-year-old boy. revealed that patients with a PR

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4 CHOI et al
TABLE 2 Laboratory and Diagnostic Findings which is not regularly seen in
MIS-C Without First- MIS-C With First- P Normal Kawasaki disease.21 More commonly,
Degree AVB Degree AVB Laboratory Values PR interval prolongation is seen in
Total patients, n 26 6 — — infections such as Lyme disease.16 In
Age, y, median (range) 7.5 (1–20) 11.5 (9–17) — — addition to the first-degree AVB
Male sex, n (%) 12 (46) 5 (83) .11 — found in our cohort of patients with
ICU admission, n (%) 21 (81) 4 (67) .46 — MIS-C, 1 patient developed a new-
Progression to advanced AVB, n 0 0 — —
(%)
onset RBBB with PR prolongation
Longest PR interval, ms 140 (80–178) 225 (200–302) ,.01 — during the acute illness phase.
Lowest LVEF percentile, median 56.5 (48–59) 53.5 (45–57) .32 — Although first-degree AVB is
(IQR) commonly seen in patients with Lyme
High-sensitive troponin T, ng/L, 44 (13–88) 89 (49–217) .11 ,14 disease and acute rheumatic fever,
median (IQR)
NT-proBNP, pg/mL, median (IQR) 7236 (3117–27 552) 5438 (1809–35 255) .90 10–242
involvement of the bundle branches is
CRP, mg/dL, median (IQR) 201 (48–300) 211 (163–255) .77 ,0.9 uncommon.22
ESR, mm/h, median (IQR) 69 (47–79) 78 (58–90) .48 0–20
Procalcitonin, ng/mL, median 1.9 (0.7–16.3) 2.6 (0.8–2.8) .79 ,0.08 At our institution, patients with MIS-C
(IQR) and first-degree AVB did not progress
Ferritin, ng/mL, median (IQR) 595 (344–866) 559 (378–752) .96 13–150 to high-degree AVB. This may be
IL-6, pg/mL, median (IQR) 227 (80–315) 124 (102–315) .85 ,5 explained by the initiation of
Manual absolute band count 4.5 (0–10) 4.5 (0–7) .71 0
percentile, median (IQR)
immunosuppression, including
D-dimer, mg/mL, median (IQR) 3.8 (2.5–8.1) 2.9 (2.2–3.9) .21 ,0.8 glucocorticoids and IVIg early in the
Fibrin, mg/dL, median (IQR) 571 (426–680) 709 (660–750) .18 191–430 acute phase of illness. Previous data
LDH, U/L, median (IQR) 373 (285–444) 308 (288–523) .99 140–280 regarding the efficacy of
Albumin, g/dL, median (IQR) 2.9 (2.5–3.5) 2.6 (2.2–3.5) .50 3.9–5.2 immunosuppression for acquired
CRP, C-reactive protein; ESR, erythrocyte sedimentation rate; IL-6, interleukin 6; LDH, lactate dehydrogenase; NT-proBNP, AVB are limited. In one study,
N-terminal pro–brain natriuretic peptide; —, not applicable.
a review of the literature indicated
that complete heart block associated
with acute myocarditis resolved in all
interval .300 milliseconds were human valvular endothelium because
3 children in whom steroids and IVIg
more likely to progress to having of the antigenic similarities of the
treatment were used.12 Literature has
complete AVB from an infectious infectious agent and the glycoproteins
also revealed that glucocorticoids
etiology process, such as Lyme of cardiac valves.19 This process may
downregulate the activation of the
disease.16 In our study, 1 patient result in mitral or aortic valvulitis as
proinflammatory response and have
developed significant PR prolongation well as pancarditis. A similar
been used to treat congenital heart
of 302 milliseconds, which improved pathophysiology of AVB has not yet
block in fetuses and neonates.23,24 We
without progression to advanced been clearly established. Cristal
suspect that the early initiation of
AVB. Additionally, AVB in patients et al20 showed that advanced AVB can
high-dose steroids and IVIg treatment
with Lyme carditis and myocarditis occur in the absence of rheumatic
may have curtailed the inflammatory
typically resolved within 7 and 5 carditis, suggesting an alternative
effects on the myocardium and
days, respectively.17,18 In our study, mechanism of acquired AVB. In this
conduction system and, therefore, the
we found that most patients’ PR vein, conduction abnormalities of
progression of first-degree AVB to
intervals returned back to baseline in MIS-C may be an isolated finding
advanced AVB.
a median of 3 days from the initial separate from the myocardial injury
diagnosis of first-degree AVB. documented in patients actively This study is inherently limited by its
infected with SARS-CoV-2.10 retrospective design and small
The exact pathogenic mechanism sample size. Furthermore, the
underlying the development of Although the clinical presentation and diagnosis of MIS-C continues to
conduction abnormalities remains conduction abnormalities found in evolve, and the symptoms may also
unknown. In patients with rheumatic patients with MIS-C share similarities overlap with other viral illnesses in
carditis, there is evidence suggesting with other disease entities, there are pediatric patients, making the
molecular mimicry as the etiology of a few notable distinctions. Despite diagnosis challenging.
myocardial injury.19 During an acute similar presenting characteristics
infection (such as group A with Kawasaki disease, including Although no patients in our study
Streptococcus), the immune response limbic sparing conjunctivitis and oral progressed to advanced AVB, 1
leads to production of antibodies or mucosal changes, patients with MIS-C patient developed significant PR
cytotoxic T cells directed against exhibited a prolonged PR interval, prolongation and 1 patient had new-

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PEDIATRICS Volume 146, number 6, December 2020 5
onset RBBB. Previous studies have up should be established to document
revealed a progression of PR interval normalization of the PR interval.
ABBREVIATIONS
prolongation to advanced AVB in AVB: atrioventricular block
other infectious or inflammatory COVID-19: coronavirus disease
conditions, such as Lyme disease.14,16 CONCLUSIONS 2019
It is possible that disease in patients This study reveals a 19% prevalence ECG: electrocardiogram
with MIS-C may theoretically have of first-degree AVB in patients IQR: interquartile range
progressed to advanced AVB in the diagnosed with MIS-C. In our subset IVIg: intravenous immunoglobulin
absence of treatment. Given the of patients, first-degree AVB LVEF: left ventricular ejection
relative lack of knowledge and associated with MIS-C improved fraction
prospective studies regarding the without progression to advanced MIS-C: multisystem inflammatory
MIS-C disease process, conclusions AVB. Cardiac enzymes, inflammatory syndrome in children
about the natural history are markers, and cardiac function were PCR: polymerase chain reaction
necessarily limited. In this vein, all not associated with first-degree AVB RBBB: right bundle branch block
patients with MIS-C should be development. Future multicenter SARS-CoV-2: severe acute respira-
monitored closely during studies are warranted to further tory syndrome
hospitalization with frequent ECGs elucidate conduction abnormalities coronavirus 2
and telemetry monitoring, and follow- associated with the novel MIS-C.

FUNDING: No external funding.

POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

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PEDIATRICS Volume 146, number 6, December 2020 7
 MIS-C and Cardiac Conduction Abnormalities
Nak Hyun Choi, Michael Fremed, Thomas Starc, Rachel Weller, Eva Cheung, Anne
Ferris, Eric S. Silver and Leonardo Liberman
Pediatrics 2020;146;
DOI: 10.1542/peds.2020-009738 originally published online November 12, 2020;

Updated Information & including high resolution figures, can be found at:
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 MIS-C and Cardiac Conduction Abnormalities
Nak Hyun Choi, Michael Fremed, Thomas Starc, Rachel Weller, Eva Cheung, Anne
Ferris, Eric S. Silver and Leonardo Liberman
Pediatrics 2020;146;
DOI: 10.1542/peds.2020-009738 originally published online November 12, 2020;

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
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